Download Down the bottleneck?

BRIAN CHARLESWORTH
SPECIATON
Down the bottleneck?
Experiments in which laboratory populations of fruitflies have been repeatedly
passed through bottlenecks fail to support 'founder-effect' models of speciation.
Most contemporary evolutionary biologists consider the
acquisition of reproductive isolation between two formerly
interbreeding populations to be the criterion for regarding
them as having achieved the status of separate species; this
is the basis of the 'biological species concept' [1,2]. Reproductive isolation may involve factors such as behavioural or
ecological differences that prevent mating of individuals
from the two populations (pre-zygotic isolation), or
genetic differences that lead to sterility or inviability of
hybrids (post-zygotic isolation) [1,2]. There is much less
agreement about the causes of speciation, largely because
data on the genetics and biogeography of species differences permit only indirect inferences about causation [3].
It seems clear, however, that a very important role in speciation has been played by the genetic divergence of two
geographically isolated populations that were formerly part
of the same breeding unit [1-3].
There are two possible ways in which such divergence may
lead to reproductive isolation. One is by the independent
substitution of new alleles at different loci in separate populations, such that each new allele is advantageous or
selectively neutral on its current genetic background. But
there is no selection pressure to ensure that the new alleles
from a pair of isolated populations will function in harmony when they are brought together in an Fl hybrid.
Incompatibilities between the mating behaviours or the
genomes of the two populations may thus eventually arise
(Fig. la), even though no selectively inferior genotypes
have ever been produced within either population [1].
The alternative possibility is that one of the populations
passes through an 'adaptive valley' of reduced fitness, as a
result of random changes in genotype frequencies due to
finite population size (genetic drift), which knock the
population off an initial equilibrium under selection (Fig.
Ib). A hybrid between the two populations will be likely
to have a genotype that corresponds to the adaptive valley,
and hence will suffer reduced fitness, giving rise to postzygotic isolation. Similarly, male and female mating behaviours might be displaced from their initial states, through
the genetic drift of alleles controlling courtship behaviour,
leading to the evolution of a new set of behaviours that
produce pre-zygotic isolation from the ancestral state.
This latter type of mechanism was first proposed by Sewall
Wright [4], who envisaged that speciation-could be a byproduct of his general 'shifting-balance' process of evolutionary change, which depends on the above type of interaction between drift and selection. In particular, he
suggested that a chromosomal rearrangement which causes
a high degree of sterility when heterozygous, such as a
reciprocal translocation, could become fixed as a result of
drift in very small populations founded by a few colonizing individuals [4]. This theory was the precursor of more
recent models of 'founder-effect' speciation [5,6]. Despite
differences in detail, these models all require a new population to be founded by a small number of individuals, and
then to grow rapidly to a large size. Genetic drift during
the initial phase of small population size can propel the
population towards a new equilibrium; once a large size
has been attained, the population will remain there under
the influence of selection.
Advocates of founder-effect speciation have suggested that
it can cause much more rapid speciation than processes
that rely on changes taking place in large populations,
Fig. 1. Two modes of speciation. (a) A
population, initially fixed for alleles A, and
B1 at two different loci, is split into two
geographically isolated populations; one
becomes fixed for new allele A2, the other
for new allele B2. Fixation of a new allele
can occur either because it has a selective
advantage, or because it is selectively neutral and fixed by drift. In an F1 hybrid
between the two populations, the two new
alleles interact to produce a selectively
inferior genotype. (b) Alleles A1 and B1 are
initially present at high frequencies. As a
result of genetic drift, one population
becomes fixed for the low-frequency
alleles A2 and B2, despite the reduced fitness of genotype A1/A2 B1/B2, which must
have been present at a high frequency in
the transitional stage before A2 and B2
became fixed. If the other population is
unchanged, the F1 hybrid between the two
populations will suffer reduced fitness.
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Current Biology 1995, Vol 5 No 9
because it overcomes conservative forces that supposedly
prevent evolutionary change in large populations [5,6].
Founder-effect speciation is also consistent with the observation that new species often evolve in association with the
colonization of new habitats [5,6]. Critics - myself included - have pointed out that population genetic theory
and data do not support the notion that large populations
are inherently incapable of evolutionary change [7]. Furthermore, theoretical models of founder events suggest that
there is only a low probability that a transition which
induces a high degree of reproductive isolation will occur
in a single founder event, and plausible alternative explanations for associations between founder events and speciation exist [3,7]. While the results of genetic analyses of the
basis of reproductive isolation strongly support the notion
that it is due to the acquisition of different sets of interacting genes in separate populations [3], they cannot tell us
the causes of such divergence, so that the question of the
role of founder events in speciation is left unanswered by
such analyses, valuable as they are in other respects.
Experimental studies on the effects of bottlenecks of small
population size seem to offer the best hope for resolving
this question. There is evidence from studies of groups like
the Hawaiian Drosophila fauna that successful founder
events are frequently associated with speciation [8]. If this is
due to the type of process outlined in Figure lb, it should
be possible to bring about significant reproductive isolation
by passing replicate laboratory populations through population bottlenecks, and testing them either for isolation
among themselves, or from control populations that have
not experienced bottlenecks. Several studies of this kind
have been published over the last 15 years, using Drosophila
or the house fly Musca domestica as material [9]. Only
sporadic instances of relatively weak reproductive isolation
have been detected in association with bottlenecks.
A very large study of this kind has recently been published
by Andres Moya and co-workers [10], again with largely
negative results. The design of their study is as follows. Large
numbers of D. pseudoobscura fruitflies from two natural populations, one in Utah and the other in Mexico, were used to
found two laboratory populations. Each ancestral population was used to initiate a number of experimental populations, with one, three, five, seven or nine pairs of founders. These were allowed to grow exponentially for six
generations, and then forced through a bottleneck of reduced numbers with crowding and competition for resources. A new cycle of founder-flush-crash events was then
restarted with the same initial number of founders; 13 such
cycles were carried out for each experimental population.
Three types of control were maintained for each of the two
ancestral populations: one in which they were not subject to
any reduction in population size, one in which they were
subject to inbreeding without flush-crash cycles, and one in
which each flush-crash cycle consisted of a generation with
a single-pair mating followed by two flush generations.
Tests for behavioural isolation between pairs of populations
were carried out by observing the numbers of different
classes of mating when 12 males and 12 females from the
two populations were placed in mating chambers. Out of a
total of 486 tests of pairs of experimental populations, 49
showed significant (p < 0.05) evidence for positive assortative mating (indicating behavioural isolation), about twice
as many as would be expected by chance; 10 out of 142
tests of isolation between experimental and control populations gave significant results. Only 1 out of 50 tests of isolation between controls was significant. Repeat tests were
conducted on pairs of populations that showed significant
isolation; there seemed to be little tendency for stable maintenance of isolation, and no evidence that isolation grew
stronger as the experimental populations were passaged
through successive founder-flush cycles. There was also no
evidence that smaller bottlenecks of population size were
associated with the acquisition of isolation, as might be
expected under the founder-effect model of speciation.
Even in those cases where isolation was highly statistically
significant, the degree of isolation was modest, and certainly
not comparable with that observed between good species.
Overall, this and earlier studies seem to suggest that measurable degrees of pre- and post-zygotic isolation are sometimes associated with population bottlenecks, but that
nothing approaching the level of isolation required for
speciation has been observed [9,10]. These experimental
tests of the effects of population bottlenecks on reproductive isolation do not seem to provide strong support for the
notion that founder events often cause speciation. Changes
in phenotypes associated with reproductive isolation, such
as mating behaviour, do seem to be weakly associated with
passages through founder-flush cycles, but this does not
prove that the population genetic mechanisms postulated
in theories of founder-effect speciation are responsible.
Indeed, partial reproductive isolation between populations
seems to be more frequently produced in the laboratory by
processes akin to the model of divergence between populations [1,2], sketched in Figure la [9]. Empirical support for
an important causal role for founder effects in speciation is
still lacking. Given the theoretical objections to this model
[3,7], scepticism towards it seems to be justified at present.
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Brian Charlesworth, Department of Ecology and Evolution,
University of Chicago, Chicago, Illinois 60637-1573, USA.